Accelerating COVID-19 Vaccination Among People Living With HIV and Health Care Workers in Tanzania: A Case Study

Within a 12-month period, targeted strategies increased COVID-19 vaccination uptake, minimized wastage of limited vaccine supply, and reduced missed opportunities for vaccination among people living with HIV and health care workers in Tanzania.


BACKGROUND
5][6] The World Health Organization (WHO) recommends COVID-19 vaccination for PLHIV. 7However, little is known about the progress toward vaccinating PLHIV outside of high-income countries.Low-income countries experienced limited supply of COVID-19 vaccines and reported lower coverage of COVID-19 vaccination compared to wealthier countries. 8At the same time, population-based studies revealed high seroprevalence of SARS-CoV-2 in sub-Saharan African countries. 9A WHO study found that two-thirds of people living in sub-Saharan Africa have been infected with SARS-CoV-2. 10 Current evidence on vaccination uptake among PLHIV mostly comes from high-income countries.In the United States, less than 6 months after COVID-19 vaccines became available, 64% of a national sample of PLHIV had received at least 1 dose of a COVID-19 vaccine. 11Other studies have also examined the willingness of PLHIV to accept COVID-19 vaccination but without determining their vaccination uptake.A cross-sectional study in Wuhan, China, found that 61% of PLHIV were willing to get vaccinated against COVID-19 compared to 81% who were willing among the general population. 12There is also limited documentation in the literature regarding the feasibility and lessons from implementing targeted vaccination strategies to reach PLHIV and other groups at higher risk of severe COVID-19 disease.
Tanzania received its first shipment of COVID-19 vaccines in July 2021 and began vaccinating an age-eligible population of adults aged 18 years and older in August 2021. 13A total of 1,058,400 doses of Janssen COVID-19 vaccine were initially made available to Tanzania through COVAX Facility coordinated by WHO as part of a donation from the U.S. Government.Other COVID-19 vaccine products were later introduced by the Government of Tanzania, including those requiring 2-dose primary series.Although the public's initial demand for the single-dose Janssen COVID-19 vaccine was high in the first few weeks of becoming accessible, the number of weekly vaccine doses administered plummeted quickly.][16] In this program case study, we describe our joint design and scale-up of COVID-19 vaccination strategies to reach PLHIV and health care workers (HCWs) in 11 regions on the mainland of Tanzania plus Zanzibar.We then quantify key programmatic achievements, provide illustrative vaccine uptake data from routine reporting among adult PLHIV in high-volume facilities, and further reflect on key lessons learned and challenges encountered.Our lessons from Tanzania may inform targeted vaccination elsewhere among populations at higher risk of severe disease in future health emergencies where vaccination becomes a countermeasure component of the public health response.

STRATEGIES TO SCALE UP COVID-19 VACCINATION AMONG PEOPLE LIVING WITH HIV AND HEALTH CARE WORKERS
An initial 6-week intensification effort to reach PLHIV and HCWs was implemented between September 27 and November 7, 2021.The intensification effort was implemented using a diverse partnership model among key stakeholders at the national-and subnational levels.The initial intensification focused on high-volume HIV clinics to: (1) expand the number of certified vaccinators, (2) create vaccination points in high-volume HIV clinics starting with administrative regions where there was strong buy-in from regional health authorities (e.g., regional medical officers and regional commissioners), (3) engage HCWs to address their concerns and build their vaccination confidence, (4) strengthen capacity of HCWs and community health workers to facilitate vaccination in facility-and community-based settings, and (5) monitor uptake of COVID-19 vaccination in high-volume facilities.Core strategies and activities from the initial intensification were expanded jointly through close collaboration with the regional health authorities, the national immunization program, and the national HIV program in Tanzania.COVID-19 vaccination activities were integrated into routine joint supportive supervision to provide real-time feedback and guidance to an expanded set of health facilities.

Expanding the Number of Certified Vaccinators
Leveraging the existing government-approved training for COVID-19 vaccination, over 3,000 HCWs were swiftly trained to become approved COVID-19 vaccinators.Expanding the number of certified vaccinators was a foundational step that subsequently allowed for the integration of fixed sites for COVID-19 vaccination within HIV clinics.Beyond the HIV clinics, HCWs in other parts of the health facilities, such as outpatient departments, also benefited from the trainings and became certified.The expanded and integrated training approach enabled the eventual expansion of COVID-19 vaccination fixed sites in multiple locations throughout health facilities, including outpatient departments.These synergistic training approaches for vaccinators from the initial intensification efforts provided a longer-term platform for refresher trainings when new COVID-19 vaccine products were added to the stock.We learned from this experience that targeting HCWs in HIV clinics provided a cost-effective entry point for subsequent expansion of COVID-19 vaccination efforts at the facility and community levels.

Creating Vaccination Points in HIV Clinics
Convenience is an important factor in enabling people to get vaccinated. 17Bringing vaccination services closer to populations in need has shown to be an effective strategy to increase vaccination uptake. 18Fixed COVID-19 vaccination points were created in HIV clinics through close collaboration among implementing partners, local government health authorities, the Immunization and Vaccine Development Program, and the National AIDS Control Program.Implementing partners worked with the facility in-charges (the most senior official responsible for health services in a designated health facility) and immunization staff at the district, regional, and central levels to coordinate vaccine supply and ensure appropriate levels of vaccine stock in the HIV clinics.We documented that having multiple vaccination points in the facility made it more convenient to get vaccinated and helped reduce wastage of multidose vials.For example, there were instances when opened vials were transported between sites in the facility to minimize wastage as and when appropriate, following localized protocols and procedures.The HCWs at different vaccination points within the same health facilities communicated with each other when they had open vials but not sufficient people present to vaccinate.Open vials were transported in small cold boxes to other vaccination points within the facility to prevent wastage.There was no standardized national or regional protocol for doing so, but HCWs came up with local simple innovations on their own to communicate and coordinate with each other.An important lesson learned is that empowering HCWs to make decisions locally can result in simple and context-appropriate innovations, as observed with local measures taken to avoid vaccine wastage in Tanzania.
The additional vaccination points in HIV clinics were not restricted to PLHIV and were appropriately leveraged to expand vaccination access, including for unvaccinated HCWs, family members of PLHIV, and others in the networks of PLHIV more broadly.We observed that the creation of COVID-19 vaccination points in HIV clinics became a best practice that was quickly replicated across all regions in Tanzania, which helped to boost nationwide uptake of COVID-19 vaccination among PLHIV, their families, and networks.

Engaging Health Care Workers and Addressing Their Concerns
The integration model leveraged teams of locally employed personnel who were already providing HIV-related supportive supervision in HIV clinics to do the same for COVID-19 vaccination.The teams were trained on evidence-based strategies to build vaccine confidence among HCWs (Supplement).This follow-up training was prompted by the low COVID-19 vaccination uptake observed among HCWs within the first 6 months of the vaccines becoming available in Tanzania.The trained team members, working in collaboration with local health authorities and facility in-charges, used a trainingof-trainers approach to meet individually with HCWs on COVID-19 vaccination to strengthen their confidence in vaccination, enable them to become active promoters of vaccination, and help them mentor other HCWs on building vaccine confidence.This was a critical strategy given that unvaccinated HCWs were not viewed as trusted communicators to promote COVID-19 vaccination.A critical lesson from this experience reinforces the need to prioritize vaccinating HCWs early so that they can be effective promoters to strengthen vaccination confidence among their clients and community members at large.

Building Capacity to Facilitate Vaccination of People Living With HIV
During scheduled HIV clinic visits, HCWs were trained to determine the COVID-19 vaccination The additional vaccination points in HIV clinics were not restricted to PLHIV and were appropriately leveraged to expand vaccination access, including for unvaccinated HCWs, family members of PLHIV, and others in the networks of PLHIV more broadly.
status of PLHIV.Unvaccinated PLHIV were counseled by HCWs and encouraged to be vaccinated.Those who agreed were vaccinated onsite at the HIV clinics.
Together with the facility in-charges, the implementing partners used a call-back strategy in which they called PLHIV who received multimonth dispensing (MMD) of antiretroviral drugs.In some facilities, in consultation with regional stakeholders, minimal transportation costs for those on MMD were reimbursed, given that they were being asked to make an extra visit to the HIV clinic outside of their scheduled visit.The call-back approach facilitated the vaccination of PLHIV on MMD and likely helped to reduce vaccination inequities among this subpopulation of PLHIV.In addition, health facilities were supported to disseminate COVID-19 vaccine educational materials in high-traffic areas to encourage patients and their families to get vaccinated.Moreover, community health workers and expert clients were trained to support the integration of COVID-19 vaccination promotion into preexisting HIV-related outreach.Community activities included addressing misinformation about vaccination and engaging PLHIV-led community-based organizations at the grassroots level.We learned that as the vaccines are being promoted, they should also made available at the same time to avoid missed opportunities for vaccination.In essence, vaccination demand and vaccine delivery efforts are optimized when they are integrated into a unified intervention bridged by HCWs.

Monitoring Uptake of COVID-19 Vaccination
A weekly aggregated Excel-based uptake monitoring system was rapidly implemented and launched initially in 124 high-volume HIV clinics by the end of September 2021.The Excel template was periodically modified and scaled up to include all 562 high-volume HIV clinics supported by the U.S. Centers for Disease Control and Prevention (CDC) in Tanzania and Zanzibar by December 2021.At the end of each week, implementing partners reported the aggregated number of PLHIV and HCWs in their supported sites who were fully vaccinated (i.e., received the recommended primary series doses for the specified vaccine product), partially vaccinated (i.e., missed 1 of the primary series doses of a multidose vaccine), unvaccinated (i.e., had not received any COVID-19 vaccine dose), or had unknown vaccination status.Adult PLHIV were defined as diagnosed people living with HIV who are aged 20 years or older and enrolled in HIV care and treatment services in a health facility supported by CDC in 11 regions on Tanzania mainland and Zanzibar.This age cut-off was used because it had existing reliable denominators across the supported HIV clinics that fed into the weekly monitoring of the proportion of PLHIV.HCWs included all clinical staff, administrative personnel, and other nonclinical staff in health facilities supported by CDC in 11 regions on the mainland of Tanzania and Zanzibar.Between September 2021 and September 2022, the proportion of fully vaccinated adult PLHIV increased from <1% to 97% and the proportion of fully vaccinated HCWs increased from 23% to 80% in the monitored facilities (Figure).
No data system existed for monitoring COVID-19 vaccination uptake among PLHIV and HCWs at the onset of the scale-up efforts.The rapidly deployed aggregated reporting system had key benefits.First, it allowed us to have weekly snapshots of the progress that implementing partners were making with vaccinating PLHIV and HCWs against targets that were assigned to them.Weekly reporting helped ensure accountability of vaccination resources and informed continuous programmatic adjustments.For example, enhanced site support, including supportive supervision visits, was undertaken in lowperforming sites.Teams visited high-performing sites and regions to observe best practices that were later shared with other sites and regions to improve overall performance.Weekly data review meetings were conducted with the implementing partners to discuss successes and jointly come up with adaptive strategies to address emerging challenges.
The weekly aggregated reporting system also encountered several challenges.Although the underlying data reported by implementing partners were coming from the official vaccination registers in the health facilities, the vaccination data for PLHIV were not centrally aggregated nationally across all HIV clinics.This issue was initially attempted to be resolved by integrating new data fields within the Chanjo COVID national electronic immunization registry to indicate COVID-19 high-risk status of vaccinated people, including HIV status and other high-risk health conditions.This approach was severely limited by incomplete data on high-risk status in the Chanjo COVID system.Therefore, as a longer-term solution, a COVID-19 vaccination module was later developed by the Government of Tanzania and integrated into the patient-level data system (CTC2) that was already being used for clinical management of PLHIV nationally.
Rapid deployment of an aggregated reporting system enabled monitoring of vaccination progress, accountability of resources, and continuous programmatic adjustments.
CTC2 is a patient-level registry owned and operated by the Government of Tanzania.It holds detailed information on HIV and TB/HIV patients.Data from CTC2 are aggregated monthly and fed into monthly reporting in the national DHIS2 platform.Chanjo COVID is an electronic patient registry developed by the Government of Tanzania specifically for managing COVID-19 vaccination records nationwide.Chanjo COVID is built upon the DHIS2 platform.Unfortunately, Chanjo COVID and CTC2 cannot directly connect and share data.To address this issue in the future, technological solutions are needed to enable electronic immunization registries like Chanjo COVID to connect with existing patientlevel registries like CTC2.Connecting the 2 systems would result in more comprehensive patient-level data to inform clinical patient management and enable the evaluation of longitudinal patient outcomes.Additionally, the lack of national unique identifiers poses a challenge as it prevents the merging of patient-level HIV data with their COVID-19 vaccination data.This limitation reinforces the larger need for accelerating the use of unique identifiers nationally.

INSIGHTS FROM INTRA-ACTION REVIEW
On July 15, 2022, an intra-action review with stakeholders was conducted to document lessons from scaling up COVID-19 vaccination to PLHIV, HCWs, and eventually the general population in CDC-supported regions in Tanzania.The workshop included participants from the Government of Tanzania, CDC, and the 4 implementing partners.Participants were divided into 6 thematic groups: (1) collaboration and coordination, (2) capacity-building, (3) data management, (4) demand creation, (5) supply chain, and (6) service delivery.The thematic groups deliberated and reported on successes, emerging improvements, and lessons learned for their respective areas.
Crosscutting themes that materialized from the group discussions included: (1) needing close partnerships and engagement of political, government, and religious leaders for planning, capacity-building, demand creation, and service delivery to enhance vaccination reach, uptake, and acceptance at community, regional, and national levels; (2) incorporating innovative strategies to address gaps in knowledge, supply chain, or service delivery, such as providing vaccination incentives, engaging peer champions, integrating with other health services, combining outreach and vaccination with mass community gatherings, and using live media coverage of vaccination and promotion; and (3) ensuring adequate preparation and planning to forecast vaccination demand, ensure timely data entry and management, and reduce vaccination wastage.The Table summarizes additional findings from the stakeholder workshop.

COMPARATIVE PROGRESS AND CONSIDERATIONS
COVID-19 vaccines became accessible around early January 2021, but initial access was mostly restricted to high-income countries.In a multicountry cohort of PLHIV, 55% had received at least 1 dose of a COVID-19 vaccine by July 2021, with better uptake in high-income countries (71%) compared to Latin America and the Caribbean (59%), South Asia (49%), Southeast Asia (41%), and sub-Saharan Africa (18%). 20A study in New York City found that 63% of PLHIV had received at least 1 dose of a COVID-19 vaccine by October 2021. 21A separate state-wide study in the state of Oregon, United States, revealed that 62% of PLHIV in the state had received at least 1 dose of a COVID-19 vaccine as of June 2021. 22COVID-19 vaccination uptake among PLHIV has been reported to be as high as 86% in Turin, Italy, based on a study conducted between November 2021 and April 2022. 23Nevertheless, it is difficult to compare PLHIV vaccination uptake across studies because of varying methods in how the data have been captured from different data collection periods.COVID-19 vaccination data are almost nonexistent among subpopulations of PLHIV, including key populations (i.e., men who have sex with men, female sex workers, and people who inject drugs).In mainland China, only 9% of men who have sex with men who were living with HIV had received any COVID-19 vaccine as of April 2021. 12o our knowledge, no prior published study has provided nationally representative estimates of COVID-19 vaccination coverage among PLHIV.To address this evidence gap, the Tanzania HIV Impact Survey 2022-2023 incorporated a module that will provide nationally representative estimates of COVID-19 vaccination coverage among PLHIV in the country. 24Vaccination coverage among key populations cannot be ascertained through the survey, and routine data on COVID-19 vaccination uptake among key populations are not available in Tanzania.To further address this evidence gap, a module on COVID-19 vaccination was integrated into 2 planned bio-behavioral surveys among men who have sex with men, female sex workers, and people who inject drugs on Tanzania's mainland and Zanzibar with data expected to be publicly available in 2025.
Leveraging existing planned surveys with key and vulnerable populations to understand their COVID-19 uptake may inform more targeted outreach strategies to ensure vaccination equity for these groups.
Additional doses of COVID-19 vaccines are now largely accessible to the general population in many parts of the world but very rarely in most of sub-Saharan Africa. 25An immunogenicity study found a COVID-19 mRNA vaccine third dose to be tolerable among PLHIV and produced a strong humoral response in PLHIV. 26In fact, additional doses of COVID-19 vaccination among PLHIV may be required to provide robust protection against severe COVID-19, 4 especially in the evolving context of SARS-CoV-2 variants of concern. 27For PLHIV with advanced HIV disease, WHO and other international regulatory bodies strongly recommend an additional dose that extends the primary series doses should be given 1-3 months after the primary series is completed. 28Targeted strategies used to reach PLHIV that we have highlighted in this article could be used to implement evidence-informed deployment strategies for additional doses of COVID-19 vaccines to PLHIV and other populations at greater risk for severe COVID-19 disease in Tanzania and elsewhere.
Going beyond COVID-19 vaccination, training HCWs in HIV clinics to vaccinate eligible adolescents with human papillomavirus (HPV) vaccination and coordinating the availability of the vaccines at the HIV clinics may help to boost HPV vaccination uptake among this population in the future.Although adult vaccination programs are limited in sub-Saharan Africa, similar approaches of integrating immunization services into other entry points and outpatient departments within health facilities can help to reach more people more conveniently with vaccines, including during future disease outbreaks where vaccines become an integral part of the public health response.Even when it may not be logistically feasible to directly integrate immunization services at alternate entry points (e.g., due to cold chain considerations), integrating vaccination screenings in multiple entry points within health facilities and making referrals to the fixed vaccination site can be done with minimal planning and without meaningfully additive costs.

CONCLUSION
We have shown that targeting COVID-19 vaccines to groups that are at greater risk of severe COVID-19 disease is a promising strategy to increase vaccine uptake, minimize wastage of limited vaccine supply, and reduce missed opportunities for vaccination.Among many important factors of our program in Tanzania, relying on a partnership model that was built on existing health services delivery platforms was essential in scaling up vaccination uptake among PLHIV and HCWs in Tanzania.Creating a strong linkage between vaccine demand and supply-side factors was critical to increasing vaccination coverage among PLHIV, as exemplified by the creation of vaccination points in HIV clinics that leveraged trusted HCWs to simultaneously promote and deliver the vaccines.Equally important, we learned that empowering HCWs to make decisions resulted in simple and context-appropriate innovations, as observed with local measures taken by HCWs to avoid vaccine wastage within their health facilities.Our experience in Tanzania can inform targeted vaccination of vulnerable groups in similar settings with strong considerations for equity, integrated programming, and maximizing public health impact in the current COVID-19 pandemic and in future health emergencies where vaccines are part of the response.

a
Tanzania Country Office, U.S. Centers for Disease Control and Prevention, Dar es Salaam, Tanzania.b Immunization and Vaccine Development, Tanzania Ministry of Health, Dar es Salaam, Tanzania.

FIGURE.
FIGURE.Trends in Percentage of PLHIV and HCWs Fully Vaccinated Against COVID-19 in Monitored Health Facilities, Mainland Tanzania and Zanzibar, October 2021-September 2022

TABLE .
Successes, Emerging Improvements, and Lessons Learned From Thematic Groups at the Stakeholder Workshop on COVID-19 Vaccination Intensification and Scale-up